Abstract
Rationale
The behavioral and reward-related effects of stimulant drugs have been studied extensively; yet the effect of stimulants on sensory processing is still relatively unknown. Prior brain imaging studies have shown that single doses of stimulant drugs increase neural function during cognitive and attentional processes. However, it is not clear if stimulant drugs such as methamphetamine (MA) affect neural responses to novel sensory stimuli, and whether these effects depend on the visual features of the stimuli.
Objective
In this study, we examined the effects of a single dose of MA (20 mg oral) on neural activation in response to visual stimuli that varied on “non-straight edges” (NSE), a low-level visual feature that quantifies curved/fragmented edges and is related to perceived image complexity.
Methods
Healthy adult participants (n = 18) completed two sessions in which they received MA and placebo in counterbalanced order before an fMRI scan where they viewed both high and low NSE images. Participants also completed measures of subjective drug effects throughout both sessions.
Results
During both sessions, high NSE images activated primary visual cortex to a greater extent than low NSE images. Further, MA increased activation only for low NSE images in three areas of visual association cortex: left fusiform, right cingulate/precuneus, and posterior right middle temporal gyrus. This interaction was unrelated to subjective drug effects.
Conclusions
These findings suggest that stimulant drugs may change the relative sensitivity of higher order sensory processing to increase visual attention when viewing less complex stimuli. Moreover, MA-induced alterations in this type of sensory processing appear to be independent of the drugs’ ability to increase feelings of well-being.
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References
Anderson BA, Kuwabara H, Wong DF, Gean EG, Rahmim A, Brašić JR, George N, Frolov B, Courtney SM, Yantis S (2016) The role of dopamine in value-based attentional orienting. Curr Biol 26(4):550–555. https://doi.org/10.1016/j.cub.2015.12.062
APA (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Publishing, Washington, DC
Ardila A, Bernal B, Rosselli M (2015) Language and visual perception associations: meta-analytic connectivity modeling of Brodmann area 37. Behav Neurol 2015:1–14. https://doi.org/10.1155/2015/565871
Arnsten AFT (2009) Toward a new understanding of attention-deficit hyperactivity disorder pathophysiology. CNS Drugs 23(Supplement 1):33–41. https://doi.org/10.2165/00023210-200923000-00005
Berman MG, Hout MC, Kardan O, Hunter MR, Yourganov G, Henderson JM, Hanayik T, Karimi H, Jonides J (2014) The perception of naturalness correlates with low-level visual features of environmental scenes. PLoS One 9(12):e114572. https://doi.org/10.1371/journal.pone.0114572
Berridge KC, Robinson TE (2016) Liking, wanting, and the incentive-sensitization theory of addiction. Am Psychol 71(8):670–679. https://doi.org/10.1037/amp0000059
Berridge CW, Waterhouse BD (2003) The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Rev 42(1):33–84
Braga RM, Sharp DJ, Leeson C, Wise RJS, Leech R (2013) Echoes of the brain within default mode, association, and heteromodal cortices. J Neurosci 33(35):14031–14039. https://doi.org/10.1523/JNEUROSCI.0570-13.2013
Briars L, Todd T (2016) A review of pharmacological management of attention-deficit/hyperactivity disorder. J Pediatr Pharmacol Ther 21(3):192–206. https://doi.org/10.5863/1551-6776-21.3.192
Courtney KE, Ghahremani DG, Ray LA (2016) The effects of pharmacological opioid blockade on neural measures of drug cue-reactivity in humans. Neuropsychopharmacology 41(12):2872–2881. https://doi.org/10.1038/npp.2016.99
Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29(3):162–173
Cox RW, Chen G, Glen DR, Reynolds RC, Taylor PA (2017) fMRI clustering and false-positive rates. Proc Natl Acad Sci U S A 114(17):E3370–E3371. https://doi.org/10.1073/pnas.1614961114
de Wit H, Crean J, Richards JB (2000) Effects of d-amphetamine and ethanol on a measure of behavioral inhibition in humans. Behav Neurosci 114(4):830–837
Eagle DM, Tufft MRA, Goodchild HL, Robbins TW (2007) Differential effects of modafinil and methylphenidate on stop-signal reaction time task performance in the rat, and interactions with the dopamine receptor antagonist cis-flupenthixol. Psychopharmacology 192(2):193–206. https://doi.org/10.1007/s00213-007-0701-7
Eklund A, Nichols TE, Knutsson H (2016) Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci U S A 113(28):7900–7905. https://doi.org/10.1073/pnas.1602413113
Haertzen CA (1966) Development of scales based on patterns of drug effects, using the addiction research center inventory (ARCI). Psychol Rep 18(1):163–194. https://doi.org/10.2466/pr0.1966.18.1.163
Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol 160:106–154
Ikeda Y, Funayama T, Tateno A, Fukayama H, Okubo Y, Suzuki H (2017) Modafinil enhances alerting-related brain activity in attention networks. Psychopharmacology 234(14):2077–2089. https://doi.org/10.1007/s00213-017-4614-9
Johanson CE, Uhlenhuth EH (1980) Drug preference and mood in humans: diazepam. Psychopharmacology 71(3):269–273. https://doi.org/10.1007/BF00433061
Jonkman LM, Kemner C, Verbaten MN, Koelega HS, Camfferman G, vd Gaag R J, …, van Engeland H (1997) Effects of methylphenidate on event-related potentials and performance of attention-deficit hyperactivity disorder children in auditory and visual selective attention tasks. Biol Psychiatry, 41(6):690–702
Kardan O, Demiralp E, Hout MC, Hunter MR, Karimi H, Hanayik T, Yourganov G, Jonides J, Berman MG (2015) Is the preference of natural versus man-made scenes driven by bottom–up processing of the visual features of nature? Front Psychol 6(471). https://doi.org/10.3389/fpsyg.2015.00471
King M, Rauch LHG, Brooks SJ, Stein DJ, Lutz K (2017) Methylphenidate enhances grip force and alters brain connectivity. Med Sci Sports Exerc 49(7):1443–1451. https://doi.org/10.1249/MSS.0000000000001252
Kotabe HP, Kardan O, Berman MG (2016) The order of disorder: deconstructing visual disorder and its effect on rule-breaking. J Exp Psychol Gen 145(12):1713–1727. https://doi.org/10.1037/xge0000240
Mayo LM, de Wit H (2015) Acquisition of responses to a methamphetamine-associated cue in healthy humans: self-report, behavioral, and psychophysiological measures. Neuropsychopharmacology 40(7):1734–1741. https://doi.org/10.1038/npp.2015.21
Morean ME, de Wit H, King AC, Sofuoglu M, Rueger SY, O’Malley SS (2013) The drug effects questionnaire: psychometric support across three drug types. Psychopharmacology 227(1):177–192. https://doi.org/10.1007/s00213-012-2954-z
Navarra R, Waterhouse B (2016) “What have we GANEd” a theoretical construct to explain experimental evidence for noradrenergic regulation of sensory signal processing. Behav Brain Sci 39:e219. https://doi.org/10.1017/S0140525X15001909
Navarra RL, Clark BD, Gargiulo AT, Waterhouse BD (2017) Methylphenidate enhances early-stage sensory processing and rodent performance of a visual signal detection task. Neuropsychopharmacology 42(6):1326–1337. https://doi.org/10.1038/npp.2016.267
Rosenberg MD, Zhang S, Hsu W-T, Scheinost D, Finn ES, Shen X, Constable RT, Li CSR, Chun MM (2016) Methylphenidate modulates functional network connectivity to enhance attention. J Neurosci 36(37):9547–9557. https://doi.org/10.1523/JNEUROSCI.1746-16.2016
Schertz KE, Sachdeva S, Kardan O, Kotabe HP, Wolf KL, Berman MG (2018) A thought in the park: the influence of naturalness and low-level visual features on expressed thoughts. Cognition 174:82–93. https://doi.org/10.1016/j.cognition.2018.01.011
Schmidt A, Müller F, Dolder PC, Schmid Y, Zanchi D, Liechti ME, Borgwardt S (2017) Comparative effects of methylphenidate, modafinil, and MDMA on response inhibition neural networks in healthy subjects. Int J Neuropsychopharmacol 20(9):712–720. https://doi.org/10.1093/ijnp/pyx037
Schultz W (2002) Getting formal with dopamine and reward. Neuron 36(2):241–263. https://doi.org/10.1016/S0896-6273(02)00967-4
Schultz W, Tremblay L, Hollerman JR (2000) Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb Cortex 10(3):272–284
Uftring S, Wachtel SR, Chu D, McCandless C, Levin DN, de Wit H (2001) An fMRI study of the effect of amphetamine on brain activity. Neuropsychopharmacology 25(6):925–935. https://doi.org/10.1016/S0893-133X(01)00311-6
Ungerleider LG, Haxby JV (1994) What’ and ‘where’ in the human brain. Curr Opin Neurobiol 4(2):157–165. https://doi.org/10.1016/0959-4388(94)90066-3
Van Hedger K, Keedy SK, Mayo LM, Heilig M, de Wit H (2018) Neural responses to cues paired with methamphetamine in healthy volunteers. Neuropsychopharmacology 43(8):1732–1737. https://doi.org/10.1038/s41386-017-0005-5
Vinberg J, Grill-Spector K (2008) Representation of shapes, edges, and surfaces across multiple cues in the human visual cortex. J Neurophysiol 99:1380–1393. https://doi.org/10.1152/jn.01223.2007
Volkow ND, Morales M (2015) The brain on drugs: from reward to addiction. Cell 162(4):712–725. https://doi.org/10.1016/j.cell.2015.07.046
Volkow ND, Wang GJ, Fowler JS, Logan J, Gatley SJ, Wong C, Hitzemann R, Pappas NR (1999) Reinforcing effects of psychostimulants in humans are associated with increases in brain dopamine and occupancy of D(2) receptors. J Pharmacol Exp Ther 291(1):409–415
Volkow ND, Wang G, Fowler JS, Logan J, Gerasimov M, Maynard L et al (2001) Therapeutic doses of oral methylphenidate significantly increase extracellular dopamine in the human brain. J Neurosci 21(2):RC121
Volkow ND, Wang G-J, Fowler JS, Telang F, Maynard L, Logan J, Gatley SJ, Pappas N, Wong C, Vaska P, Zhu W, Swanson JM (2004) Evidence that methylphenidate enhances the saliency of a mathematical task by increasing dopamine in the human brain. Am J Psychiatr 161(7):1173–1180. https://doi.org/10.1176/appi.ajp.161.7.1173
Watson DM, Hartley T, Andrews TJ (2014) Patterns of response to visual scenes are linked to the low-level properties of the image. NeuroImage 99:402–410. https://doi.org/10.1016/j.neuroimage.2014.05.045
Funding
This research is financially supported by National Institute on Drug Abuse Grant R01 DA037011 (HdW), and benefitted from S10OD018448 awarded to the University of Chicago MRI Research Center. KVH was supported by National Institute of Mental Health training grant T32MH020065. MGB was partially supported by a National Science Foundation Grant (NSF-BCS-1632445), and KES was partially supported by a NSF Graduate Research Fellowship. The funding agencies had no involvement in the research other than financial support.
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Van Hedger, K., Keedy, S.K., Schertz, K.E. et al. Effects of methamphetamine on neural responses to visual stimuli. Psychopharmacology 236, 1741–1748 (2019). https://doi.org/10.1007/s00213-018-5156-5
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DOI: https://doi.org/10.1007/s00213-018-5156-5